The transition from juvenility through maturation to senescence is a complex process that involves the regulation of longevity. Here, we identify JUNGBRUNNEN1 (JUB1), a hydrogen peroxide (H 2 O 2 )-induced NAC transcription factor, as a central longevity regulator in Arabidopsis thaliana. JUB1 overexpression strongly delays senescence, dampens intracellular H 2 O 2 levels, and enhances tolerance to various abiotic stresses, whereas in jub1-1 knockdown plants, precocious senescence and lowered abiotic stress tolerance are observed. A JUB1 binding site containing a RRYGCCGT core sequence is present in the promoter of DREB2A, which plays an important role in abiotic stress responses. JUB1 transactivates DREB2A expression in mesophyll cell protoplasts and transgenic plants and binds directly to the DREB2A promoter. Transcriptome profiling of JUB1 overexpressors revealed elevated expression of several reactive oxygen species-responsive genes, including heat shock protein and glutathione S-transferase genes, whose expression is further induced by H 2 O 2 treatment. Metabolite profiling identified elevated Pro and trehalose levels in JUB1 overexpressors, in accordance with their enhanced abiotic stress tolerance. We suggest that JUB1 constitutes a central regulator of a finely tuned control system that modulates cellular H 2 O 2 level and primes the plants for upcoming stress through a gene regulatory network that involves DREB2A.

SummaryLong-term salinity stress induces senescence, probably through an involvement of hydrogen peroxide (H2O2)-mediated signalling. This study identifies candidate H2O2-responsive cis-regulatory elements governing gene expression during salinity stress-triggered and developmental senescence.

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Graphical Abstract Highlights d Identification of genome-wide target genes for the RCO transcription factor d RCO delimits its own expression through autorepression by low-affinity binding d RCO represses local leaf growth via regulating multiple cytokinin (CK)-related genes d RCO negative autorepression fine-tunes CK activity and regulates leaf shape In Brief Hajheidari et al. identify target genes for the RCO homeodomain protein that drove leaf shape diversity. They show that RCO regulates growth via orchestrating homeostasis for the hormone cytokinin and that it also represses its own transcription via low-affinity binding sites. This autorepression helps delimit RCO expression and shape leaf form.